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Research article2020Peer reviewedOpen access

Non-cyanobacterial diazotrophs dominate nitrogen-fixing communities in permafrost thaw ponds

Fernandez, Leyden; Bertilsson, Stefan; Peura, Sari

Abstract

There is a growing concern about the implications of accelerated thawing of permafrost for regional biogeochemical cycling of carbon and other bioreactive elements. One such element of concern is nitrogen, and in this study, we investigated the diversity and biogeography of potential diazotrophs within a series of thaw ponds representing different ontogenetic stages in pond development. Using metagenomic sequence data from subarctic thaw ponds, we identified an array of nitrogenase genes across the ponds. The iron-only nitrogenase gene (anfH) was positively correlated with sulfate, while there was no correlation with methane despite previous findings that organisms carrying anfH can simultaneously participate in nitrogen fixation and methanogenesis. Sulfate is known to inhibit microbial uptake of molybdate, an element essential for the activity of the nifH (molybdenum-iron) nitrogenase and this may explain the high potential for nitrogen fixation utilizing anfH in sulfate-rich ponds. NifH was particularly abundant in the hypolimnion of the deeper and older ponds, with Deltaproteobacteria and Chlorobi as the putative dominant diazotrophs. In the epilimnetic waters, nifH composition was more variable, with various Gammaproteobacteria as abundant representatives, while cyanobacterial diazotrophs were scarce. Interestingly, nifH gene abundance was significantly positively correlated with in situ methane concentration. Based on genome-resolved metagenomics, we hypothesize that diazotrophs and methanogens engage in syntrophic interactions in anoxic waters, possibly via propionate oxidation or (in Geobacter) by interspecies electron transfer. Our results also suggest that nitrogen fixers may supply bioreactive nitrogen compounds to the thaw pond communities, thereby enhancing growth and activity of methanogens.

Published in

Limnology and Oceanography
2020, Volume: 65, number: S1, pages: S180-S193
Publisher: WILEY